Possible involvement of mitogen- and stress-activated protein kinase 1, MSK1, in metaphase-II arrest through phosphorylation of EMI2 in mouse oocytes

Developmental Biology

Volumn 359, Issue 1, 2011, Pages 73-81

  Miyagaki, Yu ^a   Kanemori, Yoshinori ^a   Baba, Tadashi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

EMI2; MAPK; Meiosis; Mouse; MSK1; Oocyte

Indexed keywords

F BOX PROTEIN; F BOX PROTEIN 43; MITOGEN ACTIVATED PROTEIN KINASE 1; SERINE; STRESS ACTIVATED PROTEIN KINASE 1; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME LOCALIZATION; GERMINAL VESICLE; IMMUNOHISTOCHEMISTRY; METAPHASE; MITOSIS SPINDLE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RESIDUE ANALYSIS; SISTER CHROMATID; UPREGULATION;

MUS;

EID: 80053585938     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.08.021     Document Type: Article

References (43)

1. Baba T., Niida Y., Michikawa Y., Kashiwabara S., Kodaira K., Takenaka M., Kohno N., Gerton G.L., Arai Y. An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. J. Biol. Chem. 1994, 269:10133-10140.
2. Bhatt R.R., Ferrell J.E. Cloning and characterization of Xenopus Rsk2, the predominant p90 Rsk isozyme in oocytes and eggs. J. Biol. Chem. 2000, 275:32983-32990.
3. Brami-Cherrier K., Roze E., Girault J.A., Betuing S., Caboche J. Role of the ERK/MSK1 signalling pathway in chromatin remodelling and brain responses to drugs of abuse. J. Neurochem. 2009, 108:1323-1335.
4. Chang H.Y., Minahan K., Merriman J.A., Jones K.T. Calmodulin-dependent protein kinase gamma 3 (CamKIIgamma3) mediates the cell cycle resumption of metaphase II eggs in mouse. Development 2009, 136:4077-4081.
5. Colledge W.H., Carlton M.B., Udy G.B., Evans M.J. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 1994, 370:65-68.
6. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
7. Deak M., Clifton A.D., Lucocq L.M., Alessi D.R. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 1998, 17:4426-4441.
8. Dumont J., Umbhauer M., Rassinier P., Hanauer A., Verlhac M.H. p90Rsk is not involved in cytostatic factor arrest in mouse oocytes. J. Cell Biol. 2005, 169:227-231.
9. Espino P.S., Li L., He S., Yu J., Davie J.R. Chromatin modification of the trefoil factor 1 gene in human breast cancer cells by the Ras/mitogen-activated protein kinase pathway. Cancer Res. 2006, 66:4610-4616.
10. Fan H.Y., Liu Z., Shimada M., Sterneck E., Johnson P.F., Hedrick S.M., Richards J.S. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 2009, 324:938-941.
11. Gross S.D., Schwab M.S., Taieb F.E., Lewellyn A.L., Qian Y.W., Maller J.L. The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90 (Rsk). Curr. Biol. 2000, 10:430-438.
12. Hashimoto N., Watanabe N., Furuta Y., Tamemoto H., Sagata N., Yokoyama M., Okazaki K., Nagayoshi M., Takeda N., Ikawa Y., Aizawa S. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 1994, 370:68-71.
13. Hauge C., Frodin M. RSK and MSK in MAP kinase signalling. J. Cell Sci. 2006, 119:3021-3023.
14. Inoue D., Ohe M., Kanemori Y., Nobui T., Sagata N. A direct link of the Mos-MAPK pathway to Erp1/Emi2 in meiotic arrest of Xenopus laevis eggs. Nature 2007, 446:1100-1104.
15. Kalab P., Kubiak J.Z., Verlhac M.H., Colledge W.H., Maro B. Activation of p90rsk during meiotic maturation and first mitosis in mouse oocytes and eggs: MAP kinase-independent and -dependent activation. Development 1996, 122:1957-1964.
16. Kawaguchi M., Fujita J., Kokubu F., Huang S.K., Homma T., Matsukura S., Adachi M., Hizawa N. IL-17F-induced IL-11 release in bronchial epithelial cells via MSK1-CREB pathway. Am. J. Physiol. Lung Cell Mol. Physiol. 2009, 296:L804-L1810.
17. Kim E., Baba D., Kimura M., Yamashita M., Kashiwabara S., Baba T. Identification of hyaluronidase, Hyal5, involved in penetration of mouse sperm through cumulus mass. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18028-18033.
18. Kimura M., Kim E., Kang W., Yamashita M., Saigo M., Yamazaki T., Nakanishi T., Kashiwabara S., Baba T. Functional roles of sperm hyaluronidase, Hyal5 and SPAM1, in fertilization in mice. Biol. Reprod. 2009, 81:939-947.
19. Kishimoto T. Cell-cycle control during meiotic maturation. Curr. Opin. Cell Biol. 2003, 15:654-663.
20. Lawitts J.A., Biggers J.D. Culture of preimplantation embryos. Methods Enzymol. 1993, 225:153-164.
21. Lefebvre C., Terret M.E., Djiane A., Rassinier P., Maro B., Verlhac M.H. Meiotic spindle stability depends on MAPK-interacting and spindle-stabilizing protein (MISS), a new MAPK substrate. J. Cell Biol. 2002, 157:603-613.
22. Madgwick S., Hansen D.V., Levasseur M., Jackson P.K., Jones K.T. Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J. Cell Biol. 2006, 174:791-801.
23. Masui Y., Markert C.L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 1971, 177:129-145.
24. Nishiyama T., Ohsumi K., Kishimoto T. Phosphorylation of Erp1 by p90rsk is required for cytostatic factor arrest in Xenopus laevis eggs. Nature 2007, 446:1096-1099.
25. Oh J.S., Han S.J., Conti M. Wee1B, Myt1, and Cdc25 function in distinct compartments of mouse oocyte to control meiotic resumption. J. Cell Biol. 2010, 188:199-207.
26. Pearce L.R., Komander D., Alessi D.R. The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 2010, 11:9-22.
27. Perry A.C., Verlhac M.H. Second meiotic arrest and exit in frogs and mice. EMBO Rep. 2008, 9:246-251.
28. Sagata N. Meiotic metaphase arrest in animal oocytes: its mechanisms and biological significance. Trends Cell Biol. 1996, 6:22-28.
29. Sasseville M., Ritter L.J., Nguyen T.M., Liu F., Mottershead D.G., Russell D.L., Gilchrist R.B. Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells. J. Cell Sci. 2010, 123:3166-3176.
30. Schmidt A., Duncan P.I., Rauh N.R., Sauer G., Fry A.M., Nigg E.A., Mayer T.U. Xenopus polo-like kinase Plx1 regulates XErp1, a novel inhibitor of APC/C activity. Genes Dev. 2005, 19:502-513.
31. Shoji S., Yoshida N., Amanai M., Ohgishi M., Fukui T., Fujimoto S., Nakano Y., Kajikawa E., Perry A.C. Mammalian Emi2 mediates cytostatic arrest and transduces the signal for meiotic exit via Cdc20. EMBO J. 2006, 25:834-845.
32. Suzuki T., Suzuki E., Yoshida N., Kubo A., Li H., Okuda E., Amanai M., Perry A.C. Mouse Emi2 as a distinctive regulatory hub in second meiotic metaphase. Development 2010, 137:3281-3291.
33. Terret M.E., Lefebvre C., Djiane A., Rassinier P., Moreau J., Maro B., Verlhac M.H. DOC1R; a MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development 2003, 130:5169-5177.
34. Tong C., Fan H.Y., Chen D.Y., Song X.F., Schatten H., Sun Q.Y. Effects of MEK inhibitor U0126 on meiotic progression in mouse oocytes: microtubule organization, asymmetric division and metaphase II arrest. Nat. Cell Res. 2003, 13:375-383.
35. Toyoda Y., Yokoyama M., Hoshi T. Studies on the fertilization of mouse eggs in vitro. Jpn. J. Anim. Reprod. 1971, 16:147-151.
36. Tsurumi C., Hoffmann S., Geley S., Graeser R., Polanski Z. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell Biol. 2004, 167:1037-1050.
37. Tung J.J., Hansen D.V., Ban K.H., Loktev A.V., Summers M.K., Adler J., Jackson P.K. A role for the anaphase-promoting complex inhibitor Emi2/XErp1, a homolog of early mitotic inhibitor 1, in cytostatic factor arrest of Xenopus eggs. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:4318-4323.
38. Tunquist B.J., Maller J.L. Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 2003, 17:683-710.
39. Verlhac M.H., Kubiak J.Z., Weber M., Graud G., Colledge W.H., Evans M.J., Maro B. Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 1996, 122:815-822.
40. Wiggin G.R., Soloaga A., Foster J.M., Murray-Tait V., Cohen P., Arthur J.S. MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol. Cell. Biol. 2002, 22:2871-2881.
41. Yamazaki T., Yamagata K., Baba T. Time-lapse and retrospective analysis of DNA methylation in mouse preimplantation embryos by live cell imaging. Dev. Biol. 2007, 304:409-419.
42. Yu L.Z., Xiong B., Gao W.X., Wang C.M., Zhong Z.S., Huo L.J., Wang Q., Hou Y., Liu K., Liu X.J., Schatten H., Chen D.Y., Sun Q.Y. MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle 2007, 6:330-338.
43. Yuan J., Xu B.Z., Qi S.T., Tong J.S., Wei L., Li M., Ouyang Y.C., Hou Y., Schatten H., Sun Q.Y. MAPK-activated protein kinase 2 is required for mouse meiotic spindle assembly and kinetochore-microtubule attachment. PloS One 2010, 28:e11247.